PAR1-activated astrocytes in the nucleus of the solitary tract stimulate adjacent neurons via NMDA receptors

Journal of Neuroscience

Volumn 35, Issue 2, 2015, Pages 776-785

  Vance, Katie M ^a   Rogers, Richard C ^a   Hermann, Gerlinda E ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Calcium imaging; Electrophysiology; Gliotransmitter; GluN2B; MEPSC; Tripartite synapse

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; AMINO ACID RECEPTOR BLOCKING AGENT; BICUCULLINE; CALCIUM GREEN 1 AM; FLUORESCENT DYE; FLUOROCITRIC ACID; GLUTAMIC ACID; IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PROTEINASE ACTIVATED RECEPTOR 1; SFLLRN NH2; SURAMIN; TCN 201; THREO BETA BENZYLOXY ASPARTATE; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; ASPARTIC ACID; BENZYLOXYASPARTATE; CALCIUM; CITRIC ACID; NR2B NMDA RECEPTOR; PEPTIDE FRAGMENT; THROMBIN RECEPTOR PEPTIDE (42-47);

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTONOMIC DYSFUNCTION; BRAIN STEM; CALCIUM TRANSPORT; CELL COMMUNICATION; CONTROLLED STUDY; EVOKED RESPONSE; IMMUNOHISTOCHEMISTRY; MOLECULAR IMAGING; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS; VOLTAGE CLAMP TECHNIQUE; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; LONG EVANS RAT; MALE; METABOLISM; MINIATURE ENDPLATE POTENTIAL; PHYSIOLOGY; SENSORY NERVE CELL; SYNAPSE; VAGUS NERVE;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; ASPARTIC ACID; ASTROCYTES; CALCIUM; CITRATES; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GLUTAMIC ACID; MALE; MINIATURE POSTSYNAPTIC POTENTIALS; NEURONS, AFFERENT; PEPTIDE FRAGMENTS; RATS; RATS, LONG-EVANS; RECEPTOR, PAR-1; RECEPTORS, N-METHYL-D-ASPARTATE; SOLITARY NUCLEUS; SYNAPSES; VAGUS NERVE;

EID: 84920972980     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3105-14.2015     Document Type: Article

References (82)

1. Accorsi-Mendonça D, Zoccal DB, Bonagamba LG, Machado BH (2013) Glial cells modulate the synaptic transmission of NTS neurons sending projections to ventral medulla of Wistar rats. Physiol Rep 1:e00080.CrossRef Medline
2. Agulhon C, Fiacco TA, McCarthy KD (2010) Hippocampal short-and longterm plasticity are not modulated by astrocyte Ca2+ signaling. Science 327:1250-1254.CrossRef Medline
3. Agulhon C, Boyt KM, Xie AX, Friocourt F, Roth BL, McCarthy KD (2013) Modulation of the autonomic nervous system and behaviour by acute glial cell Gq protein-coupled receptor activation in vivo. J Physiol 591: 5599-5609.CrossRef Medline
4. Akindipe OA, Faul JL, Vierra MA, Triadafilopoulos G, Theodore J (2000) The surgical management of severe gastroparesis in heart/lung transplant recipients. Chest 117:907-910.CrossRef Medline
5. Almonte AG, Hamill CE, Chhatwal JP, Wingo TS, Barber JA, Lyuboslavsky PN, David Sweatt J, Ressler KJ, White DA, Traynelis SF (2007) Learning and memory deficits in mice lacking protease activated receptor-1. Neurobiol Learn Mem 88:295-304.CrossRef Medline
6. Almonte AG, Qadri LH, Sultan FA, Watson JA, Mount DJ, Rumbaugh G, Sweatt JD (2013) Protease-activated receptor-1 modulates hippocampal memory formation and synaptic plasticity. J Neurochem 124:109-122.CrossRef Medline
7. Angulo MC, Kozlov AS, Charpak S, Audinat E (2004) Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 24:6920-6927.CrossRef Medline
8. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208-215.CrossRef Medline
9. Araque A, Carmignoto G, Haydon PG (2001) Dynamic signaling between astrocytes and neurons. Annu Rev Physiol 63:795-813.CrossRef Medline
10. Araque A, Martín ED, Perea G, Arellano JI, Buño W (2002) Synaptically released acetylcholine evokes Ca2+elevations in astrocytes in hippocampal slices. J Neurosci 22:2443-2450. Medline
11. Berkowitz N, Schulman LL, McGregor C, Markowitz D (1995) Gastroparesis after lung transplantation-potential role in postoperative respiratory complications. Chest 108:1602-1607.CrossRef Medline
12. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285.CrossRef Medline
13. Bonansco C, Couve A, Perea G, Ferradas CÁ, Roncagliolo M, Fuenzalida M (2011) Glutamate released spontaneously from astrocytes sets the threshold for synaptic plasticity. Eur J Neurosci 33:1483-1492.CrossRef Medline
14. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192. Medline
15. Choe KY, Olson JE, Bourque CW (2012) Taurine release by astrocytes modulates osmosensitive glycine receptor tone and excitability in the adult supraoptic nucleus. J Neurosci 32:12518-12527.CrossRef Medline
16. Clarke DD (1991) Fluoroacetate and fluorocitrate-mechanism of action. Neurochem Res 16:1055-1058.CrossRef Medline
17. Coco S, Calegari F, Pravettoni E, Pozzi D, Taverna E, Rosa P, Matteoli M, Verderio C (2003) Storage and release of ATP from Astrocytes in culture. J Biol Chem 278:1354-1362.CrossRef Medline
18. Coughlin SR (2000) Thrombin signalling and protease-activated receptors. Nature 407:258-264.CrossRef Medline
19. Edman S, McKay S, Macdonald LJ, Samadi M, Livesey MR, Hardingham GE, Wyllie DJ (2012) TCN 201 selectively blocks GluN2A-containing NMDARs in a GluN1 co-agonist dependent but non-competitive manner. Neuropharmacology 63:441-449.CrossRef Medline
20. Evans RJ, Derkach V, Surprenant A (1992) ATP mediates fast synaptic transmission in mammalian neurons. Nature 357:503-505.CrossRef Medline
21. Fellin T, Pascual O, Gobbo S, Pozzan T, Haydon PG, Carmignoto G (2004) Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43:729-743.CrossRef Medline
22. Funk GD (2010) The ‘connexin’ between astrocytes, ATP and central respiratory chemoreception. J Physiol 588:4335-4337.CrossRef Medline
23. Garrick T, Mulvihill S, Buack S, Maeda-Hagiwara M, Tache Y (1988) Intracerebroventricular pressure inhibits gastric antral and duodenal contractility but not acid-secretion in conscious rabbits. Gastroenterology 95: 26-31. Medline
24. Gingrich MB, Traynelis SF (2000) Serine proteases and brain damage-is there a link? Trends Neurosci 23:399-407.CrossRef Medline
25. Gourine AV, Kasparov S (2011) Astrocytes as brain interoceptors. Exp Physiol 96:411-416.CrossRef Medline
26. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S (2010) Astrocytes control breathing through pH-dependent release of ATP. Science 329:571-575.CrossRef Medline
27. Guard DB, Swartz TD, Ritter RC, Burns GA, Covasa M (2009a) NMDA NR2 receptors participate in CCK-induced reduction of food intake and hindbrain neuronal activation. Brain Res 1266:37-44.CrossRef Medline
28. Guard DB, Swartz TD, Ritter RC, Burns GA, Covasa M (2009b) Blockade of hindbrainNMDAreceptors containing NR2 subunits increases sucrose intake. AmJ Physiol Regul Integr Comp Physiol 296:R921-R928.CrossRef Medline
29. Guzman JN, Sánchez-Padilla J, Chan CS, Surmeier DJ (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J Neurosci 29:11011-11019.CrossRef Medline
30. Halassa MM, Haydon PG (2010) Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu Rev Physiol 72: 335-355.CrossRef Medline
31. Halassa MM, Fellin T, Haydon PG (2007) The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med 13:54-63.CrossRef Medline
32. Hamill CE, Mannaioni G, Lyuboslavsky P, Sastre AA, Traynelis SF (2009) Protease-activated receptor 1-dependent neuronal damage involves NMDA receptor function. Exp Neurol 217:136-146.CrossRef Medline
33. Han KS, Woo J, Park H, Yoon BJ, Choi S, Lee CJ (2013) Channel-mediated astrocytic glutamate release via Bestrophin-1 targets synaptic NMDARs. Mol Brain 6:4.CrossRef Medline
34. Hansen KB, Ogden KK, Traynelis SF (2012) Subunit-selective allosteric inhibition of glycine binding to NMDA receptors. J Neurosci 32:6197-6208.CrossRef Medline
35. Hara K, Harris RA (2002) The anesthetic mechanism of urethane: the effects on rotransmitter-gated ion channels. Anesth Analg 94:313-318. Medline
36. Hassel B, Paulsen RE, Johnsen A, Fonnum F (1992) Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res 576:120-124.CrossRef Medline
37. Hermann GE, Rogers RC (2009) TNF activates astrocytes and catecholaminergic neurons in the solitary nucleus: implications for autonomic control. Brain Res 1273:72-82.CrossRef Medline
38. Hermann GE, Van Meter MJ, Rood JC, Rogers RC (2009) Proteinaseactivated receptors in the nucleus of the solitary tract: evidence for glialneural interactions in autonomic control of the stomach. J Neurosci 29: 9292-9300.CrossRef Medline
39. Hermann GE, Viard E, Rogers RC (2014) Hindbrain glucoprivation effects on gastric vagal reflex circuits and gastric motility in the rat are suppressed by the astrocyte inhibitor fluorocitrate. J Neurosci 34:10488-10496.CrossRef Medline
40. Huda R, McCrimmon DR, Martina M (2013) pH modulation of glial glutamate transporters regulates synaptic transmission in the nucleus of the solitary tract. J Neurophysiol 110:368-377.CrossRef Medline
41. Junge CE, Sugawara T, Mannaioni G, Alagarsamy S, Conn PJ, Brat DJ, Chan PH, Traynelis SF (2003) The contribution of protease-activated receptor 1 to neuronal damage caused by transient focal cerebral ischemia. Proc Natl Acad Sci U S A 100:13019-13024.CrossRef Medline
42. Junge CE, Lee CJ, Hubbard KB, Zhang Z, Olson JJ, Hepler JR, Brat DJ, Traynelis SF (2004) Protease-activated receptor-1 in human brain: localization and functional expression in astrocytes. Exp Neurol 188:94-103.CrossRef Medline
43. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683-692.CrossRef Medline
44. Katz E, Protti DA, Ferro PA, Rosato Siri MD, Uchitel OD (1997) Effects of Ca2+ channel blocker neurotoxins on transmitter release and presynaptic currents at the mouse neuromuscular junction. Br J Pharmacol 121: 1531-1540.CrossRef Medline
45. Larson GM, Koch S, O’Dorisio TM, Osadchey B, McGraw P, Richardson JD (1984) Gastric response to severe head injury. Am J Surg 147:97-105.CrossRef Medline
46. Lavrentieva A, Kontakiotis T, Bitzani M, Papaioannou-Gaki G, Parlapani A, Thomareis O, Tsotsolis N, Giala MA (2008) Early coagulation disorders after severe burn injury: impact on mortality. Intensive Care Med 34:700-706.CrossRef Medline
47. Lee CJ, Mannaioni G, Yuan H, Woo DH, Gingrich MB, Traynelis SF (2007) Astrocytic control of synaptic NMDA receptors. J Physiol London 581: 1057-1081.CrossRef Medline
48. Lin LH, Moore SA, Jones SY, McGlashon J, Talman WT (2013) Astrocytes in the rat nucleus tractus solitarii are critical for cardiovascular reflex control. J Neurosci 33:18608-18617.CrossRef Medline
49. Liu Q, Wong-Riley MT (2010) Postnatal development of N-methyl-daspartate receptor subunits 2A, 2B, 2C, 2D, and 3B immunoreactivity in brain stem respiratory nuclei of the rat. Neuroscience 171:637-654.CrossRef Medline
50. Lu WY, Rhoney DH, Boling WB, Johnson JD, Johnson D, Smith TC (1997) A review of stress ulcer prophylaxis in the neurosurgical intensive care unit. Neurosurgery 41:416-425; discussion 425-426.CrossRef Medline
51. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R (2001) Proteinase-activated receptors. Pharmacol Rev 53:245-282.Medline
52. Maggio N, Shavit E, Chapman J, Segal M (2008) Thrombin induces longterm potentiation of reactivity to afferent stimulation and facilitates epileptic seizures in rat hippocampal slices: toward understanding the functional consequences of cerebrovascular insults. J Neurosci 28:732-736.CrossRef Medline
53. Maggio N, Itsekson Z, Dominissini D, Blatt I, Amariglio N, Rechavi G, Tanne D, Chapman J (2013) Thrombin regulation of synaptic plasticity: Implications for physiology and pathology. Exp Neurol 247:595-604.CrossRef Medline
54. Mannaioni G, Orr AG, Hamill CE, Yuan H, Pedone KH, McCoy KL, Berlinguer Palmini R, Junge CE, Lee CJ, Yepes M, Hepler JR, Traynelis SF (2008) Plasmin potentiates synaptic NMDA receptor function in hippocampal neurons through activation of PAR1. J Biol Chem 283:20600-20611.CrossRef Medline
55. Martín ED, Fernández M, Perea G, Pascual O, Haydon PG, Araque A, Ceña V (2007) Adenosine released by astrocytes contributes to hypoxia-induced modulation of synaptic transmission. Glia 55:36-45.CrossRef Medline
56. McDougal DH, Hermann GE, Rogers RC (2011) Vagal afferent stimulation activates astrocytes in the nucleus of the solitary tract viaAMPAreceptors: evidence of an atypical neural-glial interaction in the brainstem. J Neurosci 31:14037-14045.CrossRef Medline
57. McDougal DH, Hermann GE, Rogers RC (2013) Astrocytes in the nucleus of the solitary tract are activated by low glucose or glucoprivation: evidence for glial involvement in glucose homeostasis. Front Neurosci 7:249.CrossRef Medline
58. Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Natl Acad Sci U S A 97:4926-4931.CrossRef Medline
59. Niclou SP, Suidan HS, Pavlik A, Vejsada R, Monard D (1998) Changes in the expression of protease-activated receptor 1 and protease nexin-1 mRNA during rat nervous system development and after nerve lesion. Eur J Neurosci 10:1590-1607.CrossRef Medline
60. Nicole O, Goldshmidt A, Hamill CE, Sorensen SD, Sastre A, Lyuboslavsky P, Hepler JR, McKeon RJ, Traynelis SF (2005) Activation of proteaseactivated receptor-1 triggers astrogliosis after brain injury. J Neurosci 25:4319-4329.CrossRef Medline
61. Ogden KK, Traynelis SF (2011) New advances in NMDA receptor pharmacology. Trends Pharmacol Sci 32:726-733.CrossRef Medline
62. Oh SJ, Han KS, Park H, Woo DH, Kim HY, Traynelis SF, Lee CJ (2012) Protease activated receptor 1-induced glutamate release in cultured astrocytes is mediated by Bestrophin-1 channel but not by vesicular exocytosis. Mol Brain 5:38.CrossRef Medline
63. Olson EE, Lyuboslavsky P, Traynelis SF, McKeon RJ (2004) PAR-1 deficiency protects against neuronal damage and neurologic deficits after unilateral cerebral hypoxia/ischemia. J Cereb Blood Flow Metab 24:964-971. Medline
64. Park H, Oh SJ, Han KS, Woo DH, Park H, Mannaioni G, Traynelis SF, Lee CJ (2009) Bestrophin-1 encodes for the Ca2+-Activated anion channel in hippocampal astrocytes. J Neurosci 29:13063-13073.CrossRef Medline
65. Park H, Han KS, Oh SJ, Jo S, Woo J, Yoon BE, Lee CJ (2013) High glutamate permeability and distal localization of Best1 channel in CA1 hippocampal astrocyte. Mol Brain 6:54.CrossRef Medline
66. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte neuron signaling. Nature 369:744-747.CrossRef Medline
67. Pasti L, Volterra A, Pozzan T, Carmignoto G (1997) Intracellular calcium oscillations in astrocytes: A highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17:7817-7830. Medline
68. Perea G, Navarrete M, Araque A (2009) Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci 32:421-431.CrossRef Medline
69. Porter JT, McCarthy KD (1996) Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J Neurosci 16:5073-5081. Medline
70. Scemes E, Giaume C (2006) Astrocyte calcium waves: what they are and what they do. Glia 54:716-725.CrossRef Medline
71. Smith K (2010) Neuroscience: settling the great glia debate. Nature 468: 160-162.CrossRef Medline
72. Sodhi SS, Guo JP, Maurer AH, O’Brien G, Srinivasan R, Parkman HP (2002) Gastroparesis after combined heart and lung transplantation. J Clin Gastroenterol 34:34-39.CrossRef Medline
73. Striggow F, Riek-Burchardt M, Kiesel A, Schmidt W, Henrich-Noack P, Breder J, Krug M, Reymann KG, Reiser G (2001) Four different types of protease-activated receptors are widely expressed in the brain and are up-regulated in hippocampus by severe ischemia. Eur J Neurosci 14:595-608.CrossRef Medline
74. Tanahashi S, Yamamura S, Nakagawa M, Motomura E, Okada M (2012) Clozapine, but not haloperidol, enhances glial d-serine and L-glutamate release in rat frontal cortex and primary cultured astrocytes. Br J Pharmacol 165:1543-1555.CrossRef Medline
75. Traynelis SF, Trejo J (2007) Protease-activated receptor signaling: new roles and regulatory mechanisms. Curr Opin Hematol 14:230-235.CrossRef Medline
76. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.CrossRef Medline
77. Wang H, Ubl JJ, Reiser G (2002) Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia 37:53-63.CrossRef Medline
78. Weinstein JR, Gold SJ, Cunningham DD, Gall CM (1995) Cellularlocalization of thrombin receptor messenger RNA in rat brain-expression by mesencephalic dopaminergic neurons and codistribution with prothrombin messenger RNA. J Neurosci 15:2906-2919. Medline
79. Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-Daspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44:851-859. Medline
80. Xi G, Keep RF, Hoff JT (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5:53-63.CrossRef Medline
81. Young B, Ott L, Yingling B, McClain C (1992) Nutrition and brain injury. J Neurotrauma 9:S375-S383. Medline
82. Zhao S, Ting JT, Atallah HE, Qiu L, Tan J, Gloss B, Augustine GJ, Deisseroth K, Luo M, Graybiel AM, Feng G (2011) Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat Methods 8:745-752.CrossRef Medline